ORIGINAL ARTICLE

Craniofacial growth variations in nasal-breathing, oral-breathing, and tracheotomized children

Silvia Fuerte Bakor,a Donald H. Enlow,b Paulo Pontes,c and Noemi Grigoletto De Biased Sao~ Paulo, Brazil, and Cleveland, Ohio

Introduction: Childhood oral breathing can alter muscular balance and lead to facial deformities. No articles in the literature have reported on the alteration of facial growth patterns in patients who have received tracheoto- mies. The purpose of this study was to evaluate craniofacial developmental consequences originating from variations in breathing mechanisms in children who are nasal breathers or oral breathers, and those who have been tracheotomized. Methods: The sample was divided into 3 groups of 10 each. The nasal group had a mean age of 13.9 years, the oral group had a mean age of 12.7 years, and the tracheotomy group had a mean age of 12.8 years. The masseter and suprahyoid muscles were evaluated with electromyography. The following measurements were made: facial, maxillary, and mandibular widths; nasion-sella-gnathion angle; and facial index. Results: The tracheotomized group was similar to the nasal group for greater activity of the masseter muscles than of the suprahyoid muscles during mastication, as well as in the measurements of facial, maxillary, and mandibular widths. The oral group showed reductions in each category. The tracheotom- ized group was similar to the oral group during maximum dental occlusion for significantly higher activity of the suprahyoid muscles compared with the masseter muscles, with reductions in vertical values. Conclusions: A childhood tracheotomy might affect facial development in a way comparable with that of oral breathers, including abnormal facial growth variations. (Am J Orthod Dentofacial Orthop 2011;140:486-92)

rregular or inadequate breathing patterns can occur to a lower position in the oral cavity, and the force bal- during childhood, and variable facial growth conse- ance of the facial muscles and the tongue becomes I 1,2 5 quences can result. The effect of the breathing changed compared with nasal-breathing children. pattern on craniofacial growth has been widely The standard breathing pattern is apparently nasal,6 debated and controversial for several decades.3 The con- and oral breathing is presumed to be an adaptive cept of the functional matrix presented a logical reason resource or a habit acquired after birth, adapting to for the findings in patients with nasal obstruction by changes in nasal pathways.7 Experiments with primates ensuring that bone remodeling occurs as a response to by Harvold et al8 and Tomer and Harvold9 had the objec- the functions of facial muscles and other soft tissues.4 tive of associating orofacial muscular activity with facial This presumably explained the narrow palate and the morphogenesis. The animals were induced toward oral long face observed in patients who are chronic oral breathing by total obstruction of their nostrils with breathers. Because of oral breathing, the tongue goes silicone plugs; this resulted in an adaptive strategy for oral breathing. Responding to the new functional pat- aResearcher, Department of Otorhinolaryngology Head and Neck Surgery, Uni- tern, all animals developed some sort of , versidade Federal de S~ao Paulo, S~ao Paulo, Brazil. with subjective variations among them. This was appar- bThomas Hill Distinguished Professor Emeritus, Department of , ently an answer to nasal obstruction and resulted in Case Western Reserve University, Cleveland, Ohio. cProfessor and chief, Department of Otorhinolaryngology and Head and Neck different morphofunctional consequences. The authors Surgery, Universidade Federal de S~ao Paulo, S~ao Paulo, Brazil; president, Intena- concluded that the increase in chronic activity of some tional Federation of Otorhinolaryngological Societies. muscular groups and the postural change of the mandi- dProfessor, Department of Otorhinolaryngology Head and Neck Surgery, Univer- sidade Federal de S~ao Paulo, S~ao Paulo, Brazil; Department of Speech Pathology, ble might cause alterations in muscle development and Pontifıcia Universidade Catolica de S~ao Paulo, S~ao Paulo, Brazil. bone remodeling. The authors report no commercial, proprietary, or financial interest in the prod- Nevertheless, because of the complexity of the cause- ucts or companies described in this article. 10 Reprint requests to: Silvia Fuerte Bakor, Rua Marechal Hermes, 43, apt 111, and-effect association, authors such as McNamara, 11 12 Santo Andre, S~ao Paulo, Brazil; e-mail, [email protected]. Trotman et al, and Vig pointed out that craniofacial Submitted, August 2009; revised and accepted, November 2009. growth modifications derived from oral breathing 0889-5406/$36.00 Copyright Ó 2011 by the American Association of Orthodontists. should be analyzed more critically. There is a need for doi:10.1016/j.ajodo.2011.06.017 determining more basic and objective criteria when

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defining oral breathing as an etiologic growth-altering factor because interactions between form and function should explain any associations between oral breathing and growth, which seems to be multifactorial.12 Until now, studies were lacking in the literature concerning the morphologic and functional facial devel- opmental patterns in patients who had a tracheotomy during the facial growth period. Experiments with animals based on eliminating nasal breathing with a tracheotomy attempted to determine what facial growth changes occur when the breathing stimulus from nasal respiratory path- ways was lacking.13,14 When breathing only with the lower respiratory pathways through the trachea, the animals could remain with their lips shut and thus free from the muscular imbalances frequently associated with oral breathing. A shorter mandibular length, smaller nasal width, reduced basicranial length and facial height, smaller palatine depth, and an increased palatal plane angle were verified. Nevertheless, these experiments did not consider that the animals could develop new functional adaptations, caused by the tracheotomy, to Fig. Linear transverse measurements. maintain their vital functions. The morphologic variations that were observed in dogs during their MATERIAL AND METHODS growth might be related to the possibility that new The sample consisted of 30 patients divided into 3 functional growth adaptations occur because of the groups. The project was approved by the ethics commit- tracheotomy.14 A recent study warned that changes in tee for research of the Federal University of S~ao Paulo in the normal nasal-breathing pattern can profoundly affect Brazil. Group 1 had 10 patients (7 boys, 3 girls) with the development of the craniofacial skeleton in both a mean age of 13.9 years (SD, 2.6 years) with clinically humans and experimental animals.15 observed predominantly nasal breathing. Group 2 had Tracheotomized children do not have the breathing 10 patients (3 boys, 7 girls) with a mean age of 12.7 years stimulus from nasal pathways or the facial muscular im- (SD, 1.7 years) having predominantly oral breathing. The balances frequently associated with oral breathing. It is oral-breathing pattern diagnoses were made by clinical generally accepted that there is a relationship between and nasofibroscopic examinations by an otolaryngolo- the form and function of the craniofacial skeleton. The gist (N.G.D.B.), showing at least 1 of these affections: al- behavior of the muscles of the face seems to suffer lergic rhinitis, obstructive hypertrophy of the palatine functional variations according to different breathing and/or pharyngeal tonsils, and nasal septum deviation. patterns; therefore, the responses of craniofacial growth Group 3 had 10 patients (7 boys, 3 girls) with a tracheot- might also be variable. Surface electromyography (EMG), omy performed at an average age of 8 years 9 months; first used by Moyers,16 is a reliable method generally their mean age was 12.8 years (SD, 2.5 years), and they used for the quantitative analysis of muscular function, had no neurologic or congenital alterations, genetic syn- and it is considered an excellent and appropriate test to dromes, or craniofacial malformations. No orthodontic determine the effects of variable muscular activity on the or orthopedic procedures were performed before this functional matrix that is directly affecting facial growth. study was completed. The quantitative evaluation of the relationship between The functional analysis was determined by EMG of morphology and function is useful for adequate under- the masseter and suprahyoid muscles. This was per- standing of a growing face. Thus, it seems important to formed at the Larynx and Voice Service at the Federal study the behavior of the facial muscles relating to University of S~ao Paulo in Brazil, by using the EMG developmental adaptations in different breathing pat- unit measuring system (model MEB 9200/9300, Nihon terns on facial development. We evaluated craniofacial Kohden, Tokyo, Japan). Surface bipolar disposable consequences originating from variations in childhood electrodes were used, with a 20 3 25 mm button connec- breathing mechanisms of patients having predominantly tion, silver/silver chloride with clear auto-adhesive nasal breathing or predominantly oral breathing, or hydrogel (Spes Medica, S.r.l., Battipaglia, Italy) with an those who had a tracheotomy. interelectrode distance of 10 mm. The electromyographic

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Table I. Means and standard deviations for the root mean square values of the left and right masseter muscles in mastication and maximum dental occlusion according to the breathing groups

Nasal (n 5 10) Oral (n 5 10) Tracheo (n 5 10) Kruskal-Wallis (P) Results Masseter mastication Right Mean 130.87 76.33 163.13 0.323 Nasal 5 oral 5 tracheo SD 119.02 81.85 140.21 Left Mean 134.69 60.71 114.5 0.17 Nasal 5 oral 5 tracheo SD 174.75 66.12 87.96 Masseter occlusion Right Mean 281.16 99.61 144.24 0.613 Nasal 5 oral 5 tracheo SD 314.34 61.39 158.32 Left Mean 344.08 93.69 162.95 0.412 Nasal 5 oral 5 tracheo SD 383.25 54.93 160.75 Tracheo, Tracheotomized. activities were registered at 200 mV, with and 8-second cranial base and the mandibular plane), N-Me (linear recording for each test. The electromyographic wave sig- measurement from nasion to menton), S-Go (linear nals were processed by EMG analysis software (version measurement from sella to cephalometric gonion), and 1.01; EMG System, S~ao Jose dos Campos, Brazil). The S-Go/N-Me (facial index). calculation of the root mean square of the electrophysi- ologic potentials was provided by EMG analysis, which Statistical analysis also provided the graphs for the acquisition of the elec- The Kolmogorov-Smirnov test was applied to verify tromyographic signals generated by each muscle. the symmetry of the sample, which did not follow the The subjects, sitting upright in a dental chair, with the Gauss curve. The nonparametric Kruskal-Wallis test head supported and the Frankfort plane parallel to the was used for independent data. When differences were floor, had their electromyographic activity recorded. Elec- found, identification was made by applying the Tukey trodes were applied by the technician researcher (S.F.B.) multiple comparisons test. Comparisons between the on the skin above the bilateral bodies of the masseter masseter and suprahyoid groups during mastication and suprahyoid muscles. To determine the masseters’ were performed with Wilcoxon tests. The percentages electrode area, the patients were asked to achieve their of the relationship between the groups were calculated. maximum intercuspal force. The greatest muscular area The significance level for these tests was set at 5%. was palpated and selected, taking care that the contralateral electrodes were symmetrically positioned. RESULTS To determine the suprahyoid electrode area, the patients The Kruskal-Wallis test showed no significant differ- were asked to make movements with the tongue against ences in the EMG values for the right and left masseter the hard palate, and the greatest muscular area was muscles, mastication, or maximum dental occlusion for palpated and selected. Care was taken to use the same po- the 3 groups (Table I). Differences were identified for the sitioning of the contralateral electrodes. EMG activities at maximum dental occlusion EMG values of the left and right different functions of the stomatognathic system were suprahyoid groups. The Tukey multiple comparison test performed: habitual mastication, in which the patients verified that the oral group was like the tracheotomized chewed 3 raisins as usual on the side of their spontaneous group, although the nasal group showed less electrical ac- choice; and maximum dental occlusion, the maximum tivity in the left and right suprahyoid muscles compared voluntary clenching in the intercuspal position. with the other groups during dental occlusion (Table II). The morphologic analysis was determined with Comparisons were made between the masseter and in the frontal view, and linear transverse suprahyoid groups during mastication by using Wilcoxon measurements were made for facial width (ZL-ZR), max- tests, and there was a significant difference in the oral illary width (JL-JR), and mandibular width (A-G/G-A), as group, with higher values for electrical activity in the shown in the Figure. In the lateral view, the measure- suprahyoid group. Table III shows the means and standard ments were N-S-Gn (angle between sella, nasion, and deviations for the root mean square values of the masseter gnathion), S-N/Go-Me (angle between the anterior and suprahyoid groups on habitual mastication.

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Table II. Means and standard deviations for the root mean square values of the left and right suprahyoid muscle in mastication and maximum dental occlusion according to the breathing groups

Nasal (n 5 10) Oral (n 5 10) Tracheo (n 5 10) Kruskal-Wallis (P) Results Suprahyoid habitual mastication Right Mean 108.64 111.86 151.33 0.648 Nasal 5 oral 5 tracheo SD 106.05 131.87 145.27 Left Mean 136.17 100.38 181.06 0.468 Nasal 5 oral 5 tracheo SD 129.71 113.19 171.22 Suprahyoid maximum occlusion Right Mean 12.2 48.76 55.38 0.049* Nasal \ oral 5 tracheo (Tukey) SD 5.04 59.41 65.57 Left Mean 12.41 38.12 61.55 0.034* Nasal \ tracheo 5 oral (Tukey) SD 4.01 43.87 75.29 Tracheo, Tracheotomized. *P \0.05.

a 2.94% mean increased value compared with the nasal Table III. Means and standard deviations of the root group and a 8.26% increased value compared with the mean square values of the masseter and suprahyoid oral group. The oral group showed a mean reduction groups on habitual mastication of 5.56% compared with the nasal group for the facial Muscle group index.

Masseter Suprahyoid Wilcoxon test (P) DISCUSSION Nasal (n 510) Mean 132.78 122.40 0.575 Patients having predominantly oral breathing had SD 128.33 116.63 smaller maxillary widths, mandibular widths, and facial Oral (n 510) widths compared with nasal breathers (5%) and those Mean 68.52 106.12 0.022* who had been tracheotomized (6%). When the oral SD 73.00 119.88 Tracheo (n 510) and nasal groups were compared, our results agreed 2 Mean 138.81 166.20 0.575 with those of Linder-Aronson, Adamidis and Spyropou- SD 110.29 151.88 los,17 Hultcrantz et al,18 and Oulis et al.19 During masti- cation, it is normally expected that contraction of the Tracheo, Tracheotomized. *P \0.05. suprahyoid muscles occurs only to maintain the mouth in a slightly opened position and to perform protrusive movements, acting antagonistically to the elevator mus- The Kruskal-Wallis test verified significant differ- cles of the . This is considering that its electrical ences in maxillary, mandibular, and facial widths activity must not be higher than that from the masseter (Table IV). The Tukey test verified that the nasal group muscles.20 We compared the activities of the masseter was similar to the tracheotomized group, although the and suprahyoid muscles, with the masseter muscle of oral group showed a 5% mean reduction compared the oral group showing less activity than the suprahyoid with the nasal group and a 6% reduction compared muscle. The nasal and tracheotomized groups demon- with the tracheotomized group for maxillary, mandibu- strated greater electrical activity for the masseter mus- lar, and facial widths. cles than for the suprahyoid muscles. Oral breathing We identified significant differences in N-S-Gn induces functional adaptations to favor air passage.2 (y-axis of growth) and S-Go/N-Me index (Jarabak’s Thus, the functional adaptations of the oral breathers coefficient) (Table V). For the N-S-Gn measurement, might not happen with tracheotomized patients, with the tracheotomized group showed a mean reduced value no maxillary, mandibular, or facial narrowing. The elec- of 2.78% compared with the nasal group and a 4.74% trical activity from the masseter muscle is adequate in reduction compared with the oral group. For the S-Go/ patients with nasal breathing and in the tracheotomized N-Me (facial index), the tracheotomized group showed patients, whereas patients with an oral-breathing

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Table IV. Means and standard deviations for the facial skeletal variables on the transversal plane according to each group

Nasal (n 510) Oral (n 5 10) Tracheo (n 5 10) Kruskal-Wallis (P) Result Maxillary width Mean 67.45 64.18 68.52 0.034* Oral \ nasal 5 tracheo SD 3.61 2.78 4.48 (Tukey) Mandibular width Mean 87.17 82.78 88.27 0.049* (Tukey) SD 5.1 4.24 5 Facial width Mean 130.55 124.69 131.51 0.033* (Tukey) SD 5.21 4.44 6.5

Tracheo, Tracheotomized. *P \0.05.

Table V. Means and standard deviations for the facial skeletal variables on the vertical plane according to each group

Nasal (n 5 10) Oral (n 5 10) Tracheo (n 5 10) Kruskal-Wallis (P) Result N-S-Gn Mean 68.92 70.18 67 0.030* Oral 5 nasal . tracheo SD 2.78 3.29 2.15 (Tukey) S-N/Go-Me Mean 35.04 37.02 33.2 0.49 Oral 5 nasal 5 tracheo SD 3.78 5.43 4.66 N-Me Mean 122.88 123.69 120.22 0.625 Oral 5 nasal 5 tracheo SD 7.56 4.73 10.82 S-Go Mean 78.86 74.96 79.42 0.236 Oral 5 nasal 5 tracheo SD 7.49 4.88 8.45 S-Go/N-Me Mean 0.6411 0.6061 0.6603 0.008* Oral \ nasal 5 tracheo SD 0.0337 0.0343 0.0348 (Tukey)

Tracheo, Tracheotomized. *P \0.05. pattern have a hypo-function of the masseter muscles. in normal-breathing patients with a temporary obstruc- This might account for the maintenance of the transver- tion of the respiratory pathway. The results suggested sal measurements in patients with nasal and trecheo- that a modification of the breathing pattern can influ- tomized breathing, as well as the significant reduction ence mandibular posture as well as the activity of the of these measurements in those with oral breathing. masseter and suprahyoid muscles, in addition to the A number of researchers (Linder-Aronson,2 Adamidis anterior bundle of the temporalis and sternocleidomas- and Spyropoulos,17 Bresolin et al,21 Cheng et al,22 Per- toideus muscles. eira et al,23 Valera et al,24 and Lessa et al25) working During maximum occlusion, suprahyoid activity with oral breathers verified a clockwise mandibular rota- should be weak. The nasal group showed this pattern. tion. This implies an increase in the mandibular plane The oral group showed greater activity of the suprahyoid relative to the anterior cranial base in oral-breathing muscles during both mastication and maximum occlu- patients compared with nasal-breathing patients. In sion, a functional adaptation of the mandible’s posture our study, we also observed that the N-S-Gn angle in to favor air passage. The tracheotomized group also the oral group showed a greater clockwise rotation of showed greater activity of the suprahyoid muscles dur- the mandibular plane. Moreover, the tracheotomized ing maximum occlusion. Even if during mastication group had the smallest rotation. Using nasal plugs, the suprahyoid muscle did not show significant differ- Hellsing et al26 studied postural alterations of the man- ences among the groups, perhaps that could be identi- dible relating to the function of the masticatory muscles fied in a larger sample. On this point, more attention

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in future studies is needed. During maximum occlusion, that, after a childhood tracheotomy, it can be expected we observed that the electrical activity of the suprahyoid that future growth might affect facial development in muscles was significantly greater in the oral and tracheo- a manner comparable with that seen among oral tomized groups, although the adaptation pattern and breathers with abnormal facial growth variations. If we the muscular usage were different, as determined by anticipate such growth-affecting probabilities, this different needs. Opening the mouth to breath requires would permit clinical intervention before any defor- an increase of the activity in the anterior belly of the mities can be permanently established. digastric muscle to lower the mandible and stabilize its position; The mandible in this lower position requires the contraction of the geniohyoid muscle to maintain CONCLUSIONS the hyoid bone in position and to stabilize the nasal pathway.27 Ueda et al28 verified a significant inverse 1. Tracheotomized and nasal-breathing children relationship between masseter muscle activity and showed greater electrical activity of the masseter digastric muscle activity in patients with vertical cranio- muscle compared with the suprahyoid muscle facial morphology. The oral cavity goes through func- during mastication. This might explain the mainte- tional adaptations to optimize breathing; this can also nance of the transverse facial measurements of require postural alterations of the mandible, possibly patients with nasal and tracheotomized breathing. resulting in greater activity of the suprahyoid muscles The inverse occurred with the oral-breathing during oral breathing.28 By assuming that the increase children: the suprahyoid muscles showed greater of the electrical activity from the suprahyoid muscles is electrical activity compared with the masseter mus- more active during oral breathing because of these ad- cle during mastication, with a 5% mean reduction aptations, the same functional sequence can be applied of maxillary, mandibular, and facial widths. to the trachetomized patient. The presence of a tracheo- 2. The electrical activity from the suprahyoid muscles fi cutaneous fixation makes the hyolaryngeal dynamics in maximum dental occlusion was signi cantly more difficult, most likely requiring adaptations of the greater in the oral-breathing and tracheotomized suprahyoid muscles.29 This can explain increases of patients compared with the nasal group. electrical activity from these muscles in tracheotomized 3. The tracheotomized group showed a 2.78% reduced patients because the fixation can demand additional ef- value for N-S-Gn compared with the nasal group fort from this muscle group to overcome the obstacle.25 and a 4.75% reduced value compared with the The nasal group showed minimal electrical activity from oral group. For the facial index, the tracheotomized the suprahyoid muscless during maximum dental occlu- group showed a 2.94% increased value compared sion, probably because there was proper recruitment of with the nasal group and a 8.26% increased value the masseter muscles to perform this function. compared with the oral group. The changes in neuromuscular activity can relate to 4. Variations in breathing patterns accompany the anatomic variability that was observed. It is probable changes in orofacial neuromuscular activities, and that the sensorial feedback summons different motion this could lead to differing functional facial growth responses originating from different adaptations. Thus, remodeling adaptations. When nasal breathing the compensatory muscular function might be a partici- deviates or becomes interrupted, functional adapta- pating determinant directly involved in the growing cra- tions can result in the subsequent development of niofacial morphology as a consequence of oral or also variable facial morphologic growth pathways. tracheal breathing. Our findings show the necessity for new studies REFERENCES dealing with craniofacial consequences originating from variations in alternative breathing mechanisms. A 1. Subtelny JD. The significance of adenoid tissue in orthodontia. breathing variation such as a childhood tracheotomy Angle Orthod 1954;24:59-69. 2. Linder-Aronson S. Adenoids. Their effect on mode of breathing can thus anticipate facial growth changes compared and nasal airflow and their relationship to characteristics of the with mouth-breathing patients. The course of childhood facial skeleton and the dentition. A biometric, rhino-manometric growth becomes altered. 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